Mechanisms by which human DNA primase chooses to polymerize a nucleoside triphosphate

Biochemistry

Volumn 49, Issue 4, 2010, Pages 727-735

  Urban, Milan ^a   Joubert, Nicolas ^b   Purse, Byron W ^c   Hocek, Michal ^b   Kuchta, Robert D ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b INSTITUTE OF ORGANIC CHEMISTRY AND BIOCHEMISTRY   (Czech Republic)

^c UNIVERSITY OF DENVER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASE PAIRS; DNA POLYMERASE; DNA PRODUCTS; DNA STRANDS; HIGH FREQUENCY; HYDROGEN-BONDING PATTERNS; RNA PRIMERS; TAUTOMERIZATIONS; TEMPLATING; TRIPHOSPHATE;

DNA; GENES; HYDROGEN; NUCLEOTIDES; POLYMERIZATION; RNA;

HYDROGEN BONDS;

1,3 DIAZA 2 OXOPHENOTHIAZINE NUCLEOSIDE TRIPHOSPHATE; CYTOSINE DERIVATIVE; DEOXYRIBONUCLEOSIDE; DNA BASE; DNA PRIMASE; NUCLEOSIDE TRIPHOSPHATE; PURINE DERIVATIVE; PYRIMIDINE DERIVATIVE; UNCLASSIFIED DRUG; URIDINE TRIPHOSPHATE;

ARTICLE; BASE PAIRING; CONTROLLED STUDY; DNA TEMPLATE; HYDROGEN BOND; MOLECULAR MECHANICS; POLYMERIZATION; PRIORITY JOURNAL;

BASE PAIRING; BINDING SITES; DNA PRIMASE; DNA PRIMERS; HUMANS; HYDROGEN BONDING; KINETICS; MOLECULAR SEQUENCE DATA; NUCLEOTIDES; SUBSTRATE SPECIFICITY;

HERPES;

EID: 75149117855     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi9019516     Document Type: Article

References (45)

1. Arezi, B., and Kuchta, R. D. (2000) Eukaryotic DNA Primase. Trends Biochem. Sci. 25, 572-576.
2. Kornberg, A., and Baker, T. (1992) DNA Replication, 2nd ed., W. H. Freeman, San Francisco, CA.
3. Nethanel, T., and Kaufman, G. (1990) Two DNA Polymerases may be Required for Synthesis of the Lagging DNA Strand of Simian Virus 40. J. Virol. 64, 5912-5918.
4. Pavlov, Y. I., Frahm, C., NickMcElhinny, S. A., Niimi, A., Suzuki, M., and Kunkel, T. A. (2006) Evidence That Errors Made by DNA Polymerase alpha Are Corrected by DNA Polymerase delta. Curr. Biol. 16, 202-207.
5. McElhinny, S. A. N., Gordenin, D. A., Stith, C. M., Burgers, P. M. J., and Kunkel, T. A. (2008) Division of Labor at the Eukaryotic Replication Fork. Mol. Cell 30, 137-144.
6. Sheaff, R., and Kuchta, R. D. (1994) Misincorporation of Nucleotides by Calf Thymus DNA Primase and Elongation of Primers Containing Multiple Non-cognate Nucleotides by DNA Polymerase Alpha. J. Biol. Chem. 269, 19225-19231.
7. Ramirez-Aguilar, K. A., and Kuchta, R. D. (2004) Herpes Simplex Virus 1 DNA Primase: A Polymerase with Extraordinarily Low Fidelity. Biochemistry 43, 9084-9091.
8. Schneider, A., Smith, R. W., Kautz, A. R., Weisshart, K., Grosse, F., and Nasheuer, H. P. (1998) Primase Activity of Human DNA Polymerase alpha-Primase. Divalent Cations Stabilize the Enzyme Activity of the p48 Subunit. J. Biol. Chem. 273, 21608-21615.
9. Schneider, A., Smith, R. W., Kautz, A. R., Weisshart, K., Grosse, F., and Nasheuer, H. P. (1998) Primase Activity of Human DNA Polymerase alpha-Primase. J. Biol. Chem. 273, 21608-21615.
10. Kirk, B. W., and Kuchta, R. D. (1999) Human DNA Primase: Anion Inhibition, Manganese Stimulation, and Their Effects on in vitro Start Site Selection. Biochemistry 38, 10126-10134.
11. Zerbe, L., and Kuchta, R. D. (2002) The p58 Subunit of Human DNA Primase Is Important for Primer Initiation, Elongation, and Counting. Biochemistry 41, 4891-4900.
12. Kirk, B. W., Harrington, C., Perrino, F. W., and Kuchta, R. D. (1997) Eucaryotic DNA Primase Does Not Prefer to Synthesize Primers at Pyrimidine Rich DNA Sequences When Nucleosidse Triphosphates Are Present at Concentrations Found in Whole Cells. Biochemistry 36, 6725-6731.
13. Moore, C. L., Zivkovic, A., Engels, J., and Kuchta, R. D. (2004) Human DNA Primase Uses Watson-Crick Hydrogen Bonding Groups to Distinguish between Correct and Incorrect NTPs. Biochemistry 43, 12367-12374.
14. Moore, C. L., Chiaramonte, M., Higgins, T., and Kuchta, R. D. (2002) Synthesis of Nucleotide Analogs That Potently and Selectively Inhibit Human DNA Primase. Biochemistry 41, 14066-14075.
15. Kuchta, R. D., and Stengel, G. (2009) Mechanism and Evolution of DNA Primases. Biochim. Biophys. Acta (in press).
16. Lakshminarayan, M. I., Koonin, E. V., Leipe, D. D., and Aravind, L. (2005) Origin and Evolution of the Archaeo-Eukaryotic Primase Superfamily and Related Palm-Domain Proteins: Structural Insights and New Members. Nucleic Acids Res. 33, 3875-3896.
17. Kuchta, R. D., and Willhelm, L. (1991) Inhibition of DNA Primase by 9-beta-D-Arabinofuranosyladenosine Triphosphate. Biochemistry 30, 797-803.
18. Keller, K.E., Cavanaugh, N.A., and Kuchta, R. D. (2008) Interaction of Herpes Primase with the Sugar of a NTP. Biochemistry 47, 8977-8984.
19. Ramirez-Aguilar, K. A., Moore, C. L., and Kuchta, R. D. (2005) Herpes Simplex Virus I Primase Employs Watson-Crick Hydrogen Bonding to Identify Cognate NTPs. Biochemistry 44, 15585-15593.
20. Urban, M., Joubert, N., Hocek, M., Alexander, R. E., and Kuchta, R. D. (2009) Herpes Simplex Virus-1 DNA Primase: A Remarkably Inacurate Yet Selective Polymerase. Biochemistry 48, 10866-10881.
21. Kuchta, R. D., Mizrahi, V., Benkovic, P. A., Johnson, K. A., and Benkovic, S. J. (1987) Kinetic Mechanism of DNA Polymerase I (Klenow). Biochemistry 26, 8410-8417.
22. Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
23. Kirk, B. W., and Kuchta, R. D. (1999) Arg304 of Human DNA Primase Is a Key Contributor to Catalysis and NTP Binding: Primase and the Family X Polymerases Share Significant Sequence Homology. Biochemistry 38, 7727-7737.
24. Sandin, P., Borjesson, K., Li, H., Martensson, J., Brown, T., Wilhelmsson, L. M., and Albinsson, B. (2008) Characterization and Use of an Unprecedentedly Bright and Structurally Non-perturbing Fluorescent DNA Base Analogue. Nucleic Acids Res. 36, 157-167.
25. Sandin, P., Wilhelmsson, L. M., Lincoln, P., Powers, B. E. C., Brown, T., and Albinsson, B. (2005) Fluorescent Properties of DNA Base Analogue tC upon Incorporation into DNA - Negligible Influence of Neighbouring Bases on Fluorescence Quantum Yield. Nucleic Acids Res. 16, 5019-5025.
26. Stengel, G., Purse, B. W., Wilhelmsson, L. M., Urgan, M., and Kuchta, R. D. (2009) Ambivalent Incorporation of the Fluorescent Cytosine Analogues tC and tCo by Human DNA Polymerase alpha and Klenow Fragment. Biochemistry 48, 8271-8278.
27. Kuchta, R. D., Ilsley, D., Kravig, K. D., Schubert, S., and Harris, B. (1992) Inhibition of DNA Primase and Polymerase Alpha by Arabinofuranosylnucleoside Triphosphates and Related Compounds. Biochemistry 31, 4720-4728.
28. Zhang, S.-S., and Grosse, F. (1990) Accuracy of DNA Primase. J. Mol. Biol. 216, 475-479.
29. Stengel, G., Urban, M., Purse, B. W., and Kuchta, R. D. (2009) High Density Labeling of PCR Products with the Fluorescent Analogue tCo. Anal. Chem. 81, 9075-9081.
30. Washington, M. T., Wolfle, W. T., Spratt, T. E., Prakash, L., and Prakash, S. (2003) Yeast DNA Polymrase eta Makes Functional Contacts with the DNA Minor Groove Only at the Incoming Nucleoside Triphosphate. Proc. Natl. Acad. Sci. U.S.A. 100, 5113-5118.
31. Meyer, A. S., Blandino, M., and Spratt, T. (2004) E. coli DNA Polymerase I (Klenow Fragment) Uses a Hydrogen-Bonding Fork from Arg668 to the Primer Terminus and Incoming dNTP to Catalyze DNA Replication. J. Biol. Chem. 279, 33043-33046.
32. Kunkel, T. A. (1985) The Mutational Specificity of DNA Polymerase beta during in vitro DNA Synthesis. Production of Frameshift, Base Substitution, and Deletion Mutations. J. Biol. Chem. 260, 5787-5796.
33. Kunkel, T. A., and Alexander, P. S. (1986) The Base Substitution Fidelity of Eukaryotic DNA Polymerases. Mispairing Frequencies, Site Preferencs, Insertion Preferences, and Base Substitution by Dislocation. J. Biol. Chem. 261, 160-166.
34. Boosalis, M. S., Mosbaugh, D. W., Hamatake, R., Sugino, A., Kunkel, T. A., and Goodman,M. F. (1989) Kinetic Analysis of Base Substitution Mutagenesis by Transient Misalignment of DNAand by Miscoding. J. Biol. Chem. 264, 11360-11366.
35. Moran, S., Ren, R. X.-F., Rumney, S., and Kool, E. T. (1997) Difluorotoluene, a Nonpolar Isostere of Thymine, Codes Specifically and Efficiently for Adenine in DNA Replication. J. Am. Chem. Soc. 119, 2056-2057.
36. Morales, J. C., and Kool, E. T. (2000) Varied Molecular Interactions at the Active Sites of Several DNA Polymerases: Nonpolar Nucleoside Isosteres as Probes. J. Am. Chem. Soc. 122, 1001-1007.
37. Morales, J.C., andKool, E. T. (1998) Efficient Replication between non-Hydrogen Bonded Nucleoside Shape Analogs. Nat. Struct. Biol. 5, 950-954.
38. Kool, E. T. (2002) Active Site Tightness and Substrate Fit in DNA Replication. Annu. Rev. Biochem. 71, 191-219.
39. Beckman, J., Kincaid, K., Hocek, M., Spratt, T., Engels, J., Cosstick, R., and Kuchta, R. D. (2007) Human DNA Polymerase alpha Uses a Combination of Positive and Negative Selectivity to Polymerize Purine dNTPs with High Fidelity. Biochemistry 46, 448-460.
40. Cavanaugh, N. A., Urban, M., Beckman, J., Spratt, T., and Kuchta, R. D. (2009) Identifying the Features of Purine dNTPs that Allow Accurate and Efficient DNA Synthesis by Herpes Simplex Virus 1 DNA Polymerase. Biochemistry 48, 3554-3564.
41. Trostler, M., Delier, A., Urban, M., Beckman, J., Patro, J. N., Spratt, T., Beese, L. S., and Kuchta, R. D. (2009) Discrimination between Right and Wrong Purine dNTPs by DNA Polymerase I from Bacillus stearothermophilus. Biochemistry 48, 4633-4641.
42. Berdis, A. J., and McCutcheon, D. (2007) The Use of Non-natural Nucleotides to Probe Template-Independent DNA Synthesis. Chem-BioChem. 8, 1399-1408.
43. Zhang, X., Lee, I., and Berdis, A. J. (2005) The Use of Nonnatural Nucleotides to Probe the Contribution of Shape Complementarity and pi Electron Surface Area during DNA Polymerization. Biochemistry 44, 13101-13110.
44. Wolfle, W. T., Washington, M. T., Kool, E. T., Spratt, T., Helquist, S. A., Prakash, L., and Prakash, S. (2005) Evidence for a Watson-Crick Hydrogen Bonding Requirement in DNA Synthesis by Human DNA Polymerase kappa. Mol. Cell. Biol. 25, 7137-7143.
45. Washington, M. T., Helquist, S. A., Kool, E. T., Prakash, L., and Prakash, S. (2003) Requirement of Watson-Crick Hydrogen Bonding for DNA Synthesis by Yeast DNA Polymerase eta. Mol. Cell. Biol. 23, 5107-5112.